Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-25T04:15:55.721Z Has data issue: false hasContentIssue false

Ultrastructural and electrophysiological changes associated with K+-evoked release of neurotransmitter at the synaptic terminals of skate photoreceptors

Published online by Cambridge University Press:  02 June 2009

Harris Ripps
Affiliation:
Lions of Illinois Eye Research Institute, Department of Ophthalmology, and the Department of Anatomy and Cell Biology, University of Illinois College of Medicine, Chicago Marine Biological Laboratory, Woods Hole
Richard L. Chappell
Affiliation:
Marine Biological Laboratory, Woods Hole Department of Biological Sciences, Hunter College and the City University of New York Graduate Center, New York

Abstract

Bathing the skate retina in a Ringer solution containing a high concentration (100 mM) of potassium ions depolarized the visual cells, depleted the receptor terminals of synaptic vesicles, and suppressed completely the b-wave of the ERG and the intracellularly recorded response of horizontal cells (the S-potential). The depletion of synaptic vesicles was accompanied by a large increase in the extent of the plasma membrane resulting in distortion of the normal terminal profile, i.e. distension of the basal surface and elaborate infolding of protoplasmic extensions. Morphometric analysis showed that despite the changes in vesicle content and terminal structure, the combined linear extent of the vesicular and plasma membranes was unchanged from control (superfusion with normal Ringer solution); the increase in plasma membrane was equivalent to the observed loss of vesicular membrane. When returned to a normal Ringer solution, the terminals rapidly began to reform, and in about 10 min they were morphologically indistinguishable from receptor terminals seen in control preparations. After 30 min in the normal Ringer solution, the amount of membrane associated with the vesicles and the plasma membrane had reverted to control values, and once again the total membrane estimated morphometrically remained essentially the same. Thus, there is an efficient mechanism at the photoreceptor terminal for the recycling of vesicle membrane following exocytosis.

The K+-induced depletion of synaptic vesicles was paralleled by a precipitous loss of responsivity in both the b-wave of the ERG and the S-potential of the horizontal cells. However, after 30-min exposure to the high K+ and a return to normal Ringer solution, the recovery of electrophysiological activity followed a much slower time course from that associated with the structural changes; 60 min or longer were required for the potentials to exhibit maximum response amplitudes. It appears that the rate-limiting step in restoring normal synaptic function following massive depletion of vesicular stores is transmitter resynthesis and vesicle loading rather than vesicle recycling.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Almers, W. (1990). Exocytosis. Annual Review of Physiology 52, 607624.CrossRefGoogle ScholarPubMed
Ayoub, G.S., Korenbrot, J.I. & Copenhagen, D.R. (1989). Release of endogenous glutamate from isolated cone photoreceptors of the lizard. Neuroscience Research 10, S47–S56.Google Scholar
Bennett, M.V.L., Model, P.G. & Highstein, S.M. (1975). Stimulation-induced depletion of vesicles, fatigue of transmission of recovery processes at a vertebrate central synapse. Cold Spring Harbor Symposium in Quantitative Biology 40, 2535.Google Scholar
Brodsky, F.M. (1988). Living with clatrhin: its role in intracellular membrane traffic. Science 242, 13961402.Google Scholar
Burgoyne, R.D. (1990). Secretory vesicle-associated proteins and their role in exocytosis. Annual Review of Physiology 52, 647659.Google Scholar
Ceccarelli, B., Fesce, R., Grohovaz, F. & Hafmann, C. (1988). The effect of potassium on exocytosis of transmitter at the frog neuro-muscular junction. Journal of Physiology 401, 163168.CrossRefGoogle Scholar
Ceccarelli, B., Grohovaz, F. & Hurlbut, W.P. (1979). Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. Journal of Cell Biology 81, 178192.CrossRefGoogle ScholarPubMed
Ceccarelli, B., Haimann, C. & Fesce, R. (1987). Transmitter and vesicle turnover at the neuromuscular junction. In Cellular and Molecular Basis of Cholinergic Function, ed. Dowdall, M.J. & Hawthorne, J.N., pp. 269276. Chichester, England: Ellis Horwood Ltd.Google Scholar
Ceccarelli, B. & Hurlbut, W.P. (1980). Vesicle hypothesis of the release of qunata of acetylcholine. Physiological Reviews 60, 396441.Google Scholar
Ceccarelli, B., Hurlbut, W.P. & Mauro, A. (1972). Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. Journal of Cell Biology 54, 3038.Google Scholar
Ceccarelli, B., Hurlbut, W.P. & Mauro, A. (1973). Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. Journal of Cell Biology 57, 499524.Google Scholar
Copenhagen, D.R. & Jahr, C.E. (1989). Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341, 536539.Google Scholar
Dick, E. & Miller, R.F. (1978). Light-evoked potassium activity in mudpuppy retina: its relationship to the b-wave of the electroretinogram. Brain Research 154, 388394.Google Scholar
Dowling, J.E. & Ripps, H. (1970). Visual adaptation in the retina of the skate. Journal of General Physiology 56, 491520.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Ripps, H. (1971). S-potentials in the skate retina: Intracellular recordings during light and dark adaptation. Journal of General Physiology 58, 163189.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Ripps, H. (1973). Effect of magnesium on horizontal cell activity in the skate retina. Nature 242, 101103.Google Scholar
Dowling, J.E. & Ripps, H. (1976). Potassium and retinal sensitivity. Brain Research 107, 617622.Google Scholar
Florey, E. & Kriebel, M.E. (1988). Reversible effect of depolarization by K-proprionate on sub-miniature endplate potential to bell-miniature endplate potential ratios, on miniature endplate potential frequencies and amplitudes, and on synaptic vesicle diameters and densities in frog neuromuscular junctions. Neuroscience 27, 10551072.CrossRefGoogle ScholarPubMed
Fried, R.C. & Blaustein, M.P. (1978). Retrieval and recycling of synaptic vesicle membrane in pinched-off nerve terminals (synaptosomes). Journal of Cell Biology 78, 685700.CrossRefGoogle ScholarPubMed
Gennaro, J.F. Jr, Nastuk, W.L. & Rutherford, D.T. (1978). Reversible depletion of synaptic vesicles induced by application of high external potassium to the frog neuromuscular junction. Journal of Physiology 280, 237247.CrossRefGoogle Scholar
Giompres, P.E., Zimmerman, H. & Whittaker, V.P. (1981). Changes in the biochemical and biophysical parameters of cholinergic synaptic vesicles on transmitter release and during a subsequent period of rest. Neuroscience 6, 775785.CrossRefGoogle ScholarPubMed
Gray, E.G. & Pease, H.L. (1971). On understanding the organization of the retinal receptor synapses. Brain Research 35, 115.CrossRefGoogle ScholarPubMed
Haycock, J.W., Levy, W.B., Denner, L.A. & Cotman, C.W. (1978). Effects of elevated [K+]0 on the release of neurotransmitters from cortical synaptosomes: efflux or secretion? Journal of Neurochemistry 30, 11131125.Google Scholar
Heuser, J.E. & Reese, T.S. (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. Journal of Cell Biology 57, 315344.CrossRefGoogle ScholarPubMed
Highstein, S.M. & Bennett, M.V.L. (1975). Fatigue and recovery of transmission at the Mauthner fiber-giant fiber synapse of the hatchetfish. Brain Research 98, 229242.Google Scholar
Hinz, I. & Wernig, A. (1988). Prolonged nerve stimulation causes changes in transmitter release at the frog neuromuscular junction. Journal of Physiology 401, 557565.Google Scholar
Holtzman, E., Schacher, S., Evans, J. & Teichberg, S. (1977). Origin and fate of the membranes of secretion granules and synaptic vesicles: membrane circulation in neurons, gland cells and retinal photoreceptors. In Cell Surface Reviews: The Synthesis, Assembly and Turnover of Cell Surface Components, Vol. 4, ed. Poste, G. & Nicolson, G.L., pp. 165246. Holland: Elsevier Press.Google Scholar
Howe, P.R.C., Fenwick, E.M., Rostas, J.A.P. & Livett, B.G. (1977). Immunochemical comparison of synaptic plasma membrane and synaptic vesicle membrane antigens. Journal of Neurocytology 6, 339352.Google Scholar
Israel, M., Dunant, Y. & Manaranche, R. (1979). The present status of the vesicular hypothesis. Progress in Neurobiology 13, 237275.CrossRefGoogle ScholarPubMed
Iversen, L.L. & Bloom, F.E. (1970). Transmitter release mechanisms. Neurosciences Research Program Bulletin 8, 407420.Google Scholar
Katz, B. (1969). The Release of Neural Transmitter Substances. Liverpool: Liverpool University Press.Google Scholar
Kanaseki, T. & Kadota, K. (1969). The “vesicle in a basket.” A morphological study of the coated vesicle isolated from nerve endings of the guinea pig brain, with special reference to the mechanism of membrane movements. Journal of Cell Biology 42, 202220.CrossRefGoogle Scholar
Kaneko, A. & Shimazaki, H. (1976). Synaptic transmission from photoreceptors to bipolar and horizontal cells in the carp retina. Cold Spring Harbor Symposium in Quantitative Biology 40, 537546.CrossRefGoogle ScholarPubMed
Kirk, R.E. (1968). Experimental Design: Procedures For The Behavioral Sciences. Belmont, California: Brooks/Cole Publishing Co.Google Scholar
Kline, R.P., Ripps, H. & Dowling, J.E. (1985). Light-induced potassium fluxes in the skate retina. Neuroscience 14, 225235.Google Scholar
Koenig, J.H., Kosaka, T. & Ikeda, K. (1989). The relationship between the number of synaptic vesicles and the amount of transmitter released. Journal of Neuroscience 9, 19371942.Google Scholar
Krygier-Brevart, V., Weiss, D.G., Mehl, E., Schubert, P. & Kreutzberg, G.W. (1974). Maintenance of synaptic membranes by the fast axonal flow. Brain Research 77, 97110.Google Scholar
Lasater, E.M. & Dowling, J.E. (1982). Carp horizontal cells in culture respond selectively to L-glutamate and its agonists. Proceedings of the National Academy of Sciences of the U.S.A. 79, 936940.CrossRefGoogle ScholarPubMed
Lasater, E.M. & Dowling, J.E. & Ripps, H. (1984). Pharmacological properties of isolated horizontal and bipolar cells from the skate retina. Journal of Neuroscience 4, 19661975.Google Scholar
Lentz, T.L. (1983). Cellular membrane reutilization and synaptic vesicle recycling. Trends in Neurosciences 6, 4853.Google Scholar
Levy, C., Scherman, D. & Laduron, P.M. (1990). Axonal transport of synaptic vesicles and muscarinic receptors: Effect of protein synthesis inhibitors. Journal of Neurochemistry 54, 880885.CrossRefGoogle ScholarPubMed
Marc, R.E. & Lam, D.M.K.L. (1981). Uptake of aspartic and glutamic acid by photoreceptors in goldfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 78, 71857189.Google Scholar
McCartney, M.D. & Dickson, D.H. (1985). Photoreceptor synaptic ribbons: three-dimensional shape, orientation and diurnal (non) variation. Experimental Eye Research 41, 313321.Google Scholar
Model, P.G., Highstein, S.M. & Bennett, M.V.L. (1975). Depletion of vesicles and fatigue of transmission at a vertebrate central synapse. Brain Research 98, 209228.Google Scholar
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269271.Google Scholar
Pearse, B.M.F. (1975). Coated vesicles from pig brain: purification and biochemical characterization. Journal of Molecular Biology 97, 9398.Google Scholar
Perri, V., Sacchi, O., Raviola, E. & Raviola, G. (1972). Evaluation of the number and distribution of synaptic vesicles at cholinergic nerve-endings after sustained stimulation. Brain Research 39, 526529.CrossRefGoogle ScholarPubMed
Pysh, J.J. & Wiley, R.G. (1974). Synaptic vesicle depletion and recovery in cat sympathetic ganglia electrically stimulated in vivo. Journal of Cell Biology 60, 365374.Google Scholar
Ripps, H., Mehaffey, L. III, Siegel, I.M. & Niemeyer, G. (1989). Vincristine-induced changes in the retina of the isolated arterially-perfused cat eye. Experimental Eye Research 48, 771790.Google Scholar
Ripps, H., Shakib, M. & MacDonald, E.D. (1974). Turnover of synaptic vesicles in photoreceptor terminals of the skate. Biological Bulletin 147, 495.Google Scholar
Ripps, H., Shakib, M. & MacDonald, E.D. (1976). Peroxidase uptake by photoreceptor terminals of the skate retina. Journal of Cell Biology 70, 8696.CrossRefGoogle ScholarPubMed
Ripps, H., Shakib, M. & MacDonald, E.D. (1977). On the fate of synaptic vesicle membrane in photoreceptor terminals of the skate retina. Biological Bulletin 153, 443444.Google Scholar
Robitaille, R. & Tremblay, J.P. (1987). Incorporation of vesicular antigens into the presynaptic membrane during exocytosis at the frog neuromuscular junction: a light and electron microscopy immuno-chemical study. Neuroscience 21, 619629.Google Scholar
Sakai, H., Naka, K.-I., Chappel, R.L. & Ripps, H. (1986). Synaptic contacts in the outer plexiform layer of the skate retina. Biological Bulletin 171, 497498.Google Scholar
Schaeffer, S.F. & Raviola, E. (1975). Ultrastructural analysis of functional changes in the synaptic endings of turtle cone cells. Cold Spring Harbor Symposium in Quantitative Biology 40, 521528.Google Scholar
Schacher, S.M., Holtzman, E. & Hood, D.C. (1974). Uptake of horseradish peroxidase by frog photoreceptor synapses in the dark and the light. Nature 249, 261263.Google Scholar
Schacher, S.M., Holtzman, E. & Hood, D.C. (1976). Synaptic activity of frog retinal photoreceptors: a peroxidase uptake study. Journal of Cell Biology 70, 178192.Google Scholar
Slaughter, M.M. & Miller, R.F. (1985). Identification of a distinct synaptic glutamate receptor on horizontal cells in mudpuppy retina. Nature 314, 9697.Google Scholar
Stadler, H. & Kiene, M.-L. (1987). The life cycle of cholinergic synaptic vesicles. In Cellular and Molecular Basis of Cholinergic Function, ed. Dowdall, M.J. & Hawthorne, J.N., pp. 297302. Chichester, England: Ellis Horwood Ltd.Google Scholar
Szamier, R.B. & Ripps, H. (1983). The visual cells of the skate retina. Journal of Comparative Neurology 215, 5162.Google Scholar
Tomita, T. (1970). Electrical activity of vertebrate photoreceptors. Quarterly Reviews of Biophysics 3, 179222.Google Scholar
Townes-Anderson, E., MacLeish, P.R. & Raviola, E. (1985). Rod cells dissociated from mature salamander retina: ultrastructure and uptake of horseradish peroxidase. Journal of Cell Biology 100, 175188.Google Scholar
Trifonov, Yu A. (1968). Study of synaptic transmission between the photoreceptor and the horizontal cell using electrical stimulation of the retina. Biofizika 13, 809817.Google Scholar
Usukura, J. & Yamada, E. (1987). Ultrastructure of the synaptic ribbons in photoreceptor cells of Rana catesbiana revealed by freezeetching and freeze-substitution. Cell and Tissue Research 247, 483488.Google Scholar
Van Der Kloot, W. (1988). Acetylcholine quanta are released from vesicles by exocytosis (and why some think not). Neuroscience 24, 17.Google Scholar
Von Wedel, R.J., Carlson, S.S. & Kelly, R.B. (1981). Transfer of synaptic vesicle antigens to the presynaptic plasma membrane during exocytosis. Proceedings of the National Academy of Sciences of the U.S.A. 78, 10141018.Google Scholar
Witkovsky, P., Shakib, M. & Ripps, H. (1974). Interreceptoral junctions in the teleost retina. Investigative Ophthalmology 13, 9961009.Google Scholar
Zamora, A.J. & Ramierz, V.D. (1983). Structural changes in nerve endings of rat median eminence superfused with media rich in potassium ions. Neuroscience 10, 463473.Google Scholar
Zimmermann, H. (1979). Commentary: vesicle recycling and transmitter release. Neuroscience 4, 17731803.Google Scholar
Zimmermann, H. & Whittaker, V.P. (1974). Different recovery rates of the eletrophysiological, biochemical and morphological parameters in the cholinergic synapses of the Torpedo electric organ after stimulation. Journal of Neurochemistry 22, 11091114.CrossRefGoogle Scholar
Zucker, R.S. & Haydon, P.G. (1988). Membrane potential has no direct role in evoking neurotransmitter release. Nature 335, 360362.Google Scholar